Sound identity is represented robustly in auditory cortex during perceptual constancy

Stephen M Town,Katherine C Wood,Jennifer K Bizley

doi:10.1038/s41467-018-07237-3

Stephen M Town, Katherine C Wood + Show 1 more

Open Access

https://doi.org/10.1038/s41467-018-07237-3

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Abstract

Perceptual constancy requires neural representations that are selective for object identity, but also tolerant across identity-preserving transformations. How such representations arise in the brain and support perception remains unclear. Here, we study tolerant representation of sound identity in the auditory system by recording neural activity in auditory cortex of ferrets during perceptual constancy. Ferrets generalize vowel identity across variations in fundamental frequency, sound level and location, while neurons represent sound identity robustly across acoustic variations. Stimulus features are encoded with distinct time-courses in all conditions, however encoding of sound identity is delayed when animals fail to generalize and during passive listening. Neurons also encode information about task-irrelevant sound features, as well as animals’ choices and accuracy, while population decoding out-performs animals’ behavior. Our results show that during perceptual constancy, sound identity is represented robustly in auditory cortex across widely varying conditions, and behavioral generalization requires conserved timing of identity information.

Highlights

Perceptual constancy requires neural representations that are selective for object identity, and tolerant across identity-preserving transformations
We asked if tolerant representations for complex sounds exist in early auditory cortex during perceptual constancy, how tolerance was related to behavior, and how tolerance was modulated by attention and experience
We found that tolerant representations of sound identity exist during perceptual constancy, and that the timing of information about vowel identity is associated with behavioral performance

Summary

Introduction

Perceptual constancy requires neural representations that are selective for object identity, and tolerant across identity-preserving transformations. Tolerance is observed within auditory cortex, where neurons remain informative about the identity of vocalizations[18,19,20], pure tones[21] and pulse trains[22] across variations in acoustic properties For speech sounds such as vowels, multiple sound features including phoneme identity, location and F0 modulate activity of auditory cortical neurons[23,24,25,26]. We asked if tolerant representations for complex sounds exist in early auditory cortex during perceptual constancy, how tolerance was related to behavior, and how tolerance was modulated by attention and experience To address these questions, we recorded auditory cortical neurons in ferrets discriminating synthesized vowel sounds that varied across identity-preserving acoustic transformations including F0, sound location, level, and voicing. The ability of auditory cortex to represent vowel identity exceeds animals’ behavior, and requires neither training, nor task engagement

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